4-hydroxynonenal, a product of lipid peroxidation, damages cholinergic neurons and impairs visuospatial memory in rats

Journal of Neuropathology and Experimental Neurology

Volumn 57, Issue 3, 1998, Pages 257-267

  Bruch Keller, Annadora J ^a   Li, Ying Jie ^a   Lovell, Mark A ^a,b   Kraemer, Philipp J ^b   Gary, Devin S ^a   Brown, Russel R ^b   Markesbery, William R ^a,b   Mattson, Mark P ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Alzheimer disease; Choline acetyltransferase; Hippocampus; Iron; Morris water maze

Indexed keywords

4 HYDROXYNONENAL; CHOLINE ACETYLTRANSFERASE; FERROUS CHLORIDE; MALONALDEHYDE; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; FOREBRAIN; HIPPOCAMPUS; LIPID PEROXIDATION; MALE; MAZE TEST; NERVE CELL DEGENERATION; NERVE CELL LESION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; SPATIAL MEMORY; VISUAL MEMORY;

EID: 0031917723     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1097/00005072-199803000-00007     Document Type: Article

References (71)

1. Benzi G, Moretti A. Age-and peroxidative stress-related modifications of the cerebral enzymatic activities linked to mitochondria and the glutathione system. Free Radic Biol Med 1995;19:77-101
2. Mattson, MP. Cellular actions of β-amyloid precursor protein, and its soluble and fibrillogenic peptide deivatives. Physiol Rev 1997; 77:1081-1132
3. Smith MA, Sayre LM, Monnier VM, Perry G. Radical AGEing in Alzheimer's disease. Trends Neurosci 1995;18:172-76
4. Yankner BA. Mechanisms of neuronal degeneration in Alzheimer's disease. Neuron 1996;16:921-32
5. Smith CD, Carney JM, Starke-Reed PE, Oliver CN, Stadtman ER, Floyd RA, Markesbery WR. Excess brain protein oxidation and enzyme dysfunction in normal aging and in Alzheimer disease. Proc Natl Acad Sci USA 1991;88:10540-43
6. Lovell MA, Ehmann WD, Butler SM, Markesbery WR. Elevated thiobarbituric acid-reactive substances and antioxidant enzyme activity in the brain in Alzheimer's disease. Neurology 1995;45: 1594-1601
7. Moccoci P, MacGarvey MS, Beal MF. Oxidative damage to mitochondrial DNA is increased in Alzheimer's disease. Ann Neurol 1994;36:747-51
8. Smith MA, Taneda S, Richey PL, Miyata S, Yan SD, Stern D, Sayre LM, Monnier VM, Perry G. Advanced maillard reaction end products are associated with Alzheimer disease pathology. Proc Natl Acad Sci USA 1994;91:5710-14
9. Vitek MP, Bhattacharya K, Glendening JM, Stopa E, Vlassara H, Bucala R, Manogue K, Cerami A. Advanced glycation end products contribute to amyloidosis in Alzheimer disease. Proc Natl Acad Sci USA 1994;91:4766-70
10. Yan S-D, Chen X, Schmidt A-M, et al. Glycated tau protein in Alzheimer disease: A mechanism for induction of oxidant stress. Proc Natl Acad Sci USA 1994;91:7787-91
11. Cai X, Golde T, Younkin S. Release of excess amyloid β protein from a mutant amyloid β protein precursor. Science 1993;259:514-16
12. Citron M, Oltersdorf T, Haass C, et al. Mutation of the betaamyloid precursor protein in familial Alzheimer's disease increases beta-protein production. Nature 1992;360:672-74
13. 717) mutants. Science 1994;264:1336-40
14. Games D, Adams D, Alessandrinl R, et al. Alzheimer-type neuropathology in transgenic mice overexpressing V717F β-amyloid precursor protein. Nature 1995;373:523-27
15. Hsaio K, Chapman P, Nilsen S, Eckman C, Harigaya Y, Younkin S, Yang F, Cole G. Correlative memory deficits, Aβ elevation, and amyloid plaques in transgenic mice. Science 1996;274:99-103
16. Mattson MP, Cheng B, Davis D, Bryant K, Lieberburg I, Rydel RE. β-amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity. J Neurosci 1992; 12:376-89
17. Busciglio J, Lorenzo A, Yeh J, Yankner BA. β-amyloid fibrils induce tau phosphorylation and loss of microtubule binding. Neuron 1995;14:879-88
18. Butterfield DA, Hensley K, Harris M, Mattson MP, Carney J. β-amyloid peptide free radical fragments initiate synaptosomal lipoperoxidation in a sequence-specific fashion: implications to Alzheimer's disease. Biochem Biophys Res Commun 1994;200:710-715
19. Behl C, Davis J, Lesley R, Schubert D. Hydrogen peroxide mediates amyloid β protein toxicity. Cell 1994;77:817-27
20. 2+ homeostasis and cell death. J Neurosci 1995;15:6239-49
21. Keller JN, Pang Z, Geddes JW, Begley JG, Germeyer A, Waeg G, Mattson MP. Impairment of glucose and glutamate transport and induction of mitochondrial oxidative stress and dysfunction in synaptosomes by amyloid β-peptide: Role of the lipid peroxidation product 4-hydroxynonenal. J Neurochem 1997;69:273-84
22. Mark RJ, Pang Z, Geddes JW, Uchida K, Mattson MP. Amyloid β-peptide impairs glucose uptake in hippocampal and cortical neurons: Involvement of membrane lipid peroxidation. J Neurosci 1997;17:1046-54
23. Kelly J, Furukawa K, Barger SW, Mark RJ, Rengen MR, Roth G, Mattson MP Amyloid β-peptide disrupts carbachol-induced muscarinic cholinergic signal transduction in cortical neurons. Proc Natl Acad Sci USA 1996;93:6753-58
24. Esterbauer H, Schaur RJ, Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Rad Biol Med 1991;11:81-128
25. Montine KS, Olson SJ, Amarnath V, Whetsell WO, Graham DG, Montine, TJ. Immunohistochemical detection of 4-hydroxy-2-no-nenal adducts in Alzheimer's disease is associated with inheritance of ApoE4. Am J Pathol 1997;150:437-43
26. Lovell MA, Ehmann WD, Markesbery WR. Elevated 4-hydroxy-nonenal in ventricular fluid in Alzheimer's disease. Neurobiol Aging 1997;18:457-61
27. Sayre LM, Zelasko DA, Harris PLR, Perry G, Salomon RG, Smith MA.4-hydroxynonenal-derived advanced lipid peroxidation end products are increased in Alzherimer's disease. J Neurochem 1997; 68:2092-97
28. Montine TJ, Amarnath V, Martin ME, Strittmatter WJ, Graham DG. E-4-hydroxy-2-nonenal is cytotoxic and cross-links cytoskeletal proteins in P19 neuroglial cultures. Am J Pathol 1996;148:89-93
29. Kinter M, Roberts RJ. Glutathione consumption and glutathione peroxidase inactivation in fibroblast cell lines by 4-hydroxy-2-nonenal. Free Radic Biol Med 1996;21:457-62
30. Mark RJ, Lovell MA, Markesbery WR, Uchida K, Mattson MP. A role for 4-hydroxynonenal in disruption of ion homeostasis and neuronal death induced by amyloid β-peptide. J Neurochem 1997b; 68:255-64
31. Kruman I, Bruce AJ, Bredesen DE, Waeg G, Mattson MP. Evidence that 4-hydroxynonenal mediates oxidative stress-induced neuronal apoptosis. J Neurosci 1997;17:5089-5100
32. Bartus RT, Dean RL, Beer B, Lippa AS. The cholinergic hypothesis of geriatric memory dysfunction. Science 1982;217:408-17
33. Katzman R. Alzheimer's disease. New Engl J Med 1986;314:964-73
34. Nabeshima T . Behavioral aspects of choinergic transmission: Role of basal forebrain cholinergic system in learning and memory. Prog Brain Res 1993;98:405-11
35. Kametani H, Spangler EL, Bresnahan EL, Kobayashi S, Long JM, Ingram DK. Impaired acquisition in a 14-unit T-maze following medial septal lesions in rats is correlated with lesion size and hippocampal acetylcholinesterase staining. Physiol Behav 1993;53: 221-28
36. Torres EM, Perry TA, Blockland A, Wilkinson LS, Wiley RG, Lappi DA, Dunnet SB. Behavioural, histochemical and biochemical consequences of selective immunolesions in discrete regions of the basal forebrain cholinergic system. Neuroscience 1994;63:95-122
37. Baxter MG, Bucci DJ, Gorman LK, Wiley RG, Gallagher M. Selective immunotoxic lesions of basal forebrain cholinergic cells: Effects on learning and memory in rats. Behav Neurosci 1995;109: 714-22
38. McAlonan GM, Wilkinson LS, Robbins TW, Everitt BJ. The effects of AMPA-induced lesions of the septo-hippocampal cholinergic projection on aversive conditioning to explicit and contextual cues and spatial learning in the water maze. Eur J Neurosci 1995;7:281-92
39. Paxinos G, Watson C. The rat brain in stereotaxic coordinates, 2nd ed. Sydney: Academic Press, 1986
40. Oakman SA, Faris PL, Kerr PE, Cozzari C, Hartman BK. Distribution of pontomesencephalic cholinergic neurons projecting to substantia nigra differs significantly from those projecting to ventral tegmental area. J Neurosci 1995;15:5859-69
41. Springer JE, Azbill RD, Mark RJ, Begley JG, Waeg G, Mattson MP. 4-hydroxynonenal, a lipid peroxidation product, rapidly accumulates following spinal cord injury and inhibits glutamate uptake. J Neurochem 1997;68:2469-76
42. Morales MA, Holmberg K, Xu ZQ, et al. Localization of choline acetyltransferase in rat peripheral sympathetic neurons and its coexistence with nitric oxide synthase and neuropeptides. Proc Natl Acad Sci USA 1995;92:11819-823
43. Waeg G, Dimsity G, Esterbauer H. Monoclonal antibodies for the detection of 4-hydroxynonenal modified proeteins. Free Radic Res Commun 1996;25:149-59
44. Shea PA, Aprison MN. An enzymatic method for measuring picomole quantities of acetylcholine and choline in CNS tissue. Anal Biochem 1973;56:165-177
45. Smith-Swintosky VL, Kraemer PJ, Bruce AJ, et al. Bacterial alkaloids mitigate seizure-induced hippocampal damage and memory deficits. Exp Neurol 1996;141:287-96
46. Kraemer PJ, Randall CK. Spatial learning in preweanling rats trained in a Morris water maze: Psychobiology 1995;23:144-52
47. Kraemer PJ, Brown RW, Baldwin SA, Scheff SW. Validation of a single-day Morris water maze procedure used to assess cognitive deficits associated with brain damage. Brain Res Bull 1996;39:17-22
48. Kovachich GB, Mishra OP. Lipid peroxidation in rat cortical slices as measured by the thiobarbituric acid test. J Neurochem 1980;35: 1449-52
49. 2+ injection. J Neurochem 1984;42:976-80
50. Willmore LF, Triggs WJ, Gray JD. The role of iron-induced hippocampal peroxidation in acute epileptogenesis. Brain Res 1986; 382:422-426
51. Smith GJ, Dunkley WL. Initiation of lipid peroxidation by a reduced metal ion. Arch Biochem Biophys 1962;98:46-48
52. Zhang Y, Tatsuno T, Carney J, Mattson MP. Basic FGF, NGF, and IGFs protect hippocampal neurons against iron-induced degeneration. J Cerebral Blood Flow Metab 1993;13:378-88
53. Goodman Y, Bruce AJ, Cheng B, Mattson MP. Estrogens attenuate and corticosterone exacerbates excitotoxicity, oxidative injury and amyloid β-peptide toxicity in hippocampal neurons. J Neurochem 1996;66:1836-44
54. Good PF, Perl DP, Bierer LM, Schmeidler J. Selective accumulation of aluminum and iron in the neurofibrillary tangles of Alzheimer's disease: A laser microprobe (LAMMA) study. Ann Neurol 1992; 31:286-92
55. Deibel MA, Ehmann WD, Markesbery WR. Copper, iron, and zinc imbalances in severely degenerated brain regions in Alzheimer's disease: Possible relation to oxidative stress. J Neurol Sci 1996; 143:137-42
56. Kala SV, Hasinoff BB, Richardson JS. Brain samples from Alzheimer's patients have elevated levels of loosely bound iron. Int J Neurosci 1996;86:263-69
57. Smith MA, Harris PLR, Sayre LM, Beckman JS, Perry G. Widespread peroxynitrite-mediated damage in Alzheimer's disease. J Neurosci 1997;17:2653-57
58. Mattson MP, Fu W, Waeg G, Uchida K. 4-hydroxynonenal, a product of lipid peroxidation, inhibits dephosphorylation of the microtubuleassociated protein tau. NeuroReport 1997;8:2275-81
59. Dunnett SB, Whishaw IQ, Jones GH, Bunch ST. Behavioral, biochemical and histochemical effects of different neurotoxic amino acids injected into nucleus basalis magnocellularis of rats. Neuroscience 1987;20:653-69
60. Page KJ, Everitt BJ, Robbins TW, Marston HM, Wilkinson LS. Dissociable effects on spatial maze and passive avoidance acquisition and retention following AMPA-and ibotenic acid-induced excitotoxic lesions of the basal forebrain in rats: Differential dependence on cholinergic neuronal loss. Neuroscience 1991;43:457-72
61. Winkler J, Thal LJ. Effects of nerve growth factor treatment on rats with lesions of the nucleus basalis magnocellularis produced by ibotenic acid, quisqualic acid, and AMPA. Exp Neurol 1995;136: 234-50
62. Gulyaeva NV, Lazareva NA, Libe ML, Mitrokhina OS, Onufriev MV, Stepanichev MYu, Chernysevskaya IA, Walsh TJ. Oxidative stress in the brain following intraventricular administration of ethylcholine aziridinium (AF64A). Brain Res 1996;726:174-80
63. Wortwein G, Stackman RW, Walsh TJ. Vitamin E prevents the place learning deficit and the cholinergic hypofunction induced by AF64A. Exp Neurol 1994;125:15-21
64. Pedersen WA, Kloczewiak,MA Blusztajn JK. Amyloid β-protein reduces acetylcholine synthesis in a cell line derived from cholinergic neurons of the basal forebrain. Proc Natl Acad Sci USA 1996; 93:8068-71
65. q/11. J. Neurochem 1997;69; 570-80
66. Berger-Sweeney J, Heckers S, Mesulam MM, Wiley RG, Lappi D, Sharma, M. Differential effects on spatial navigation of immunotoxin-induced cholinergic lesions of the medial septal area and nucleus basalis magnocellularis. J Neurosci 1994;14:4507-19
67. Nakamura S, Ohno T. Spatial learning impairment in aged rats: Comparing between aged basal forebrain lesioned and normal aged rats. Behav Brain Res 1996;70:69-76
68. Morris RGM. Development of a water maze procedure for studying spatial learning in the rat. J Neurosci Meth 1984;11:47-60
69. Morris RGM, Garrud P, Rawlins JNP, O'Keefe J. Place navigation is impaired in rats with hippocampal lesions. Nature 1982;297:681-83
70. Fischer W, Wictorin K, Bjorklund A, Williams LR, Varon S, Gage FH. Amelioration of cholinergic neuron atrophy and spatial memory impairment in aged rats by nerve growth factor. Nature 1987; 329:65-68
71. Ikegami S, Nihonmatsu I, Hatanaka H, Takei N, Kawamura H. Transplantation of septal cholinergic neurons to the hippocampus improves memory impairments of spatial learning in rats treated with AF64A. Brain Res 1989;496:321-26